Indiscriminate males: mating behaviour of a marine snail compromised by a sexual conflict?

Background: In promiscuous species, male fitness is expected to increase with repeated matings in an open-ended fashion (thereby increasing number of partners or probability of paternity) whereas female fitness should level out at some optimal number of copulations when direct and indirect benefits still outweigh the costs of courtship and copulation. After this fitness peak, additional copulations would incur female fitness costs and be under opposing selection. Hence, a sexual conflict over mating frequency may evolve in species where females are forced to engage in costly matings. Under such circumstance, if females could avoid male detection, significant fitness benefits from such avoidance strategies would be predicted.

Methodology/principal Findings: Among four Littorina species, one lives at very much higher densities and has a longer mating season than the other three species. Using video records of snail behaviour in a laboratory arena we show that males of the low-density species discriminate among male and female mucous trails, trailing females for copulations. In the high-density species, however, males fail to discriminate between male and female trails, not because males are unable to identify female trails (which we show using heterospecific females), but because females do not, as the other species, add a gender-specific cue to their trail.

Conclusions/significance: We conclude that there is likely a sexual conflict over mating frequency in the high-density species (L. saxatilis) owing to females most likely being less sperm-limited in this species. This has favoured the evolution of females that permanently or optionally do not release a cue in the mucus to decrease excessive and costly matings resulting in unusually high frequencies of male-male copulating attempts in the wild. This is one of few examples of masking gender identity to obtain fewer matings.